A Global Perspective on the Influence of Environmental Exposures on the Nervous System
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nature.com/brain-disorders REVIEW OPEN A global perspective on the influence of environmental exposures on the nervous system Desire Tshala-Katumbay1,2,3, Jean-Claude Mwanza4, Diane S. Rohlman5,6, Gladys Maestre7 & Reinaldo B. Oriá8 Economic transitions in the era of globalization warrant a fresh look at the neurological risks associated with environmental change. These are driven by industrial expansion, transfer and mobility of goods, climate change and population growth. In these contexts, risk of infectious and non-infectious diseases are shared across geographical boundaries. In low- and middle-income countries, the risk of environmentally mediated brain disease is augmented several fold by lack of infrastructure, poor health and safety regulations, and limited measures for environmental protection. Neurological disorders may occur as a result of direct exposure to chemical and/or non-chemical stressors, including but not limited to, ultrafine particulate matters. Individual sus- ceptibilities to exposure-related diseases are modified by genetic, epigenetic and metagenomic factors. The existence of several uniquely exposed populations, including those in the areas surrounding the Niger Delta or north western Amazon oil operations; those working in poorly regulated environments, such as artisanal mining industries; or those, mostly in sub-Saharan Africa, re- lying on cassava as a staple food, offers invaluable opportunities to advance the current understanding of brain responses to en- vironmental challenges. Increased awareness of the brain disorders that are prevalent in low- and middle-income countries and investments in capacity for further environmental health-related research are positive steps towards improving human health. Nature 527, S187-S192 (19 November 2015), DOI: 10.1038/nature16034 This article has not been written or reviewed by Nature editors. Nature accepts no responsibility for the accuracy of the information provided. eports from the World Health Organization (WHO) indicate that scientists and neuroscientists, as well as programme officers at the US the global burden of disease is determined by patterns of disease National Institutes of Health and US National Institute of Environmen- R and disability in low- and middle-income countries (LMICs), tal Health Sciences (NIEHS), and Fogarty International Center. This which, predictably, have their own environmental signatures (http:// Review integrates the goals and approaches to environmental health www.who.int/healthinfo/global_burden_disease/about/en/). How- research as per the NIEHS 2012–2017 strategic plan (https://www. ever, the effect of such signatures on both brain health and region or niehs.nih.gov/about/strategicplan/). global disability-adjusted life years (DALYs) remains unknown and needs to be added to the agenda of global environmental health re- ENVIRONMENTAL EXPOSURE AND BRAIN HEALTH search. As for high-income countries, environmental health research LMICs are home to around 80–85% of the world’s population1. Of these programmes in LMICs must primarily focus on elucidating the entire 5.8 billion people2, 1 billion remain in extreme poverty, living below the range and source of exposures to define the human ‘exposome’ (the US$1.25 per day poverty line3. Around 3 billion people do not have piped measure of all the exposures of an individual in their lifetime and how drinking water in their home and 173 million people rely on the direct these exposures relate to health) relevant to brain health in LMICs. The use of surface water. Without proper sanitation, about one billion con- research agenda should also include mechanistic and translational re- tinue to defecate in gutters, in the open bush or in open water bodies4. search, as well as capacity building to foster a new generation of envi- Wildfires and deforestation are commonplace and drought and floods, ronmental health scientists. possibly due to climate change, degrade the existing farming systems and create food insecurity5–7. Armed conflicts and population displace- SCOPE ments impose a toll on human life8. Industrial expansion coexists with In this Review, we focus on environmental risk factors for brain diseases an unprecedented rise in artisanal mining and unprotected labour9. and conditions in LMICs (http://data.worldbank.org/about/country- In some instances, normal urbanization operations, such as road con- and-lending-groups). An iterative search of the literature was con- struction and quarantines (for example during Ebola outbreaks in the ducted using PubMed to retrieve information related to environmental Democratic Republic of the Congo) have created conditions that exac- determinants and mechanisms of brain disease in LMICs. Additional erbated the risk of environmental exposure and brain disease10. Flawed opinion was obtained from interviews with leading environmental regulations compounded by a lack of infrastructure set the stage for 1Department of Neurology, Oregon Health & Science University, Portland, Oregon, 97239, USA. 2National Institute of Biomedical Research, 1197 Kinshasa I, Congo. 3Department of Neurology, University of Kinshasa, 825 Kinshasa XI, Congo. 4Department of Ophthalmology, University of North Carolina at Chapel Hill, North Carolina 27599, USA. 5Occupational and Environmental Health, The University of Iowa, Iowa 52242, USA. 6Oregon Institute of Occupational Health Sciences, Oregon Health and Science University, Portland, Oregon, 97239, USA. 7G. H. Sergievsky Center, Columbia University Medical Center, New York, New York 10032, USA. 8Department of Morphology and Institute of Biomedicine, Faculty of Medicine, Federal University of Ceara, Fortaleza 60020, Brazil. Correspondence should be addressed to D. T.-K. e-mail: [email protected]. 527 | 7578 | 19 November 2015 S187 ENVIRONMENTAL EXPOSURES | TSHALA-KATUMBAY ET AL. Table 1 | Heavy metals and exposure-related outcomes Heavy metal Source of exposure Susceptibility window Neurological outcomes Proposed mechanisms Lead76–78 Lead-contaminated dust, lead-based Lifelong Visual and verbal memory decline, Disruption of neurotransmitter paint, soil, drinking water, air, leaded intellectual deficits, decline in release and function, and prenatal gasoline, toys and lead-contaminated executive functioning (fine motor disruption of neuronal migration and sweets function, hand-eye coordination and differentiation; aggravating factors reaction time) and hyperactivity in include poor nutrition (deficiency in children iron, zinc and calcium) and younger age Mercury79,80 Mining industry, power plants, From neural development to Ataxia in adults and language, Oxidative stress or impairment of crematoria, charcoal industry, and neurulation, and adolescence attention, and visuospatial intracellular calcium and glutamate contaminated food (mostly sea food) performance deficits in children homeostasis and water Arsenic80,81 Contaminated food and drinking 5–15 years Impaired selective and focused Oxidative stress or disruption of water, air and arsenic-based attention and long-term memory metabolism of neurotransmitters treatments in children, and sensorimotor polyneuropathy Copper82 Contaminated drinking water and Children Alzheimer’s disease, OCD, ADHD, Oxidative stress, microglia food, uncoated copper cookware and Those over 65 antisocial behaviour and anxiety in cell activation or promotion of infant formula containing copper children α-synuclein and fibril formation Cobalt82,83 Contaminated drinking water and Prenatal, young children and the Optic, auditory and peripheral Alteration of mitochondrial oxidative food, inhalation of dust containing elderly neuropathy, motor deficits and verbal phosphorylation or depletion of cobalt particles in various industries memory loss neurotransmitters Cadmium83 Fumes or dust, cigarette smoke, and Prenatal, young children and the Antisocial behaviour and attention Oxidative damage and contaminated food and water elderly impairment in children, parkinsonism neurotransmitter disruption and peripheral neuropathy Manganese76,79 Airborne as fumes, aerosols or Childhood and the elderly Reduced IQ, impaired verbal learning Disruption of mitochondrial suspended particulate matter and and working and immediate memory respiratory chain reaction; contaminated water in children, and Parkinson-like aggravating factors include iron symptoms deficiency and impaired biliary excretion (liver injury or disease) Aluminium84 Contaminated air, water and food, Lifelong Alzheimer’s pathology in the form of Disruption of mitochondrial cosmetics (such as antiperspirants), neurofibrillary tangles respiratory chain reaction or metal industries and pharmaceuticals inflammation; zinc deficiency acknowledged as an aggravating factor ADHD, attention-deficit hyperactivity disorder; OCD, obsessive compulsive disorder. environmental degradation and pollution to pose serious threats — of a as tapioca), the grass pea Lathyrus sativus or the seeds from the cycad chemical or non-chemical nature — to human health. The degradation plants, which are all known to be associated with a high burden of neu- of local ecosystems leads to the creation of ‘microenvironments’ that rodisabilities at a population level17–22. Populations with unique expo- have a high risk of harmful exposures, often resulting in unique chal- sures and risks include those living in the tropical cassava belt of Ango- lenges and increased risk of human disease (Fig. 1). la, the Central African Republic, Cameroon, Congo, Tanzania, Uganda, Nigeria and Mozambique23–30;